Energy harvesting capability of lipid-merocyanine macromolecules: A new design and performance model development

Article abstract of DOI:10.1111/php.12193

Light induced cis/trans isomerization in the family of merocyanine (MC) dyes offers a recyclable proton pumping ability which can potentially be used in hybrid bio-electronic devices. In this article, a hexadecyl MC dye is embedded in lipid molecules to make a macromolecular configuration of a lipid/hexadecyl MC membrane. Lipid molecules play a critical role in stabilizing the dye in a membrane structure for practical use in energy devices. In this study, we first examined the proton pumping characteristic of the lipid/hexadecyl MC membrane in a conventional photoelectrochemical cell. Next, a major modification in the cell was introduced by eliminating I₂/I-electrolyte which resulted in a two-fold increase in the open circuit voltage compared with that of the conventional cell. In addition, the charging time in the new cell was reduced approximately four orders of magnitude. This research demonstrated that the newly designed lipid- MC cell can act as a promising bioelectronic device based on the green energy of photoinduced MC dye proton pumping. Capacitor charging time reduced and open circuit voltage enhanced significantly in the newly designed lipid-merocyanine photoelectrochemical cell.

Full text of DOI:10.1111/php.12193

Photochemistry and Photobiology, 2014, 90: 517–521
Energy Harvesting Capability of Lipid-Merocyanine Macromolecules: A
New Design and Performance Model Development
Lobat Tayebi1,2, Masoud Mozafari1, Rita El-khouri3, Parvaneh Rouhani4 and Daryoosh Vashaee*4
1School of Material Science and Engineering, Helmerich Advanced Technology Research Center, Oklahoma State
University, Tulsa, OK
2School of Chemical Engineering, Oklahoma State University, Stillwater, OK
3Department of Chemistry, University of California, Davis, CA
4School of Electrical and Computer Engineering, Helmerich Advanced Technology Research Center, Oklahoma State
University, Tulsa, OK
Received 4 September 2013, accepted 16 October 2013, DOI: 10.1111/php.12193
ABSTRACT
It has been demonstrated that the generation of thermal- and
photodriven pmf results in trans-membrane proton pumping
across a macromolecular thin-film doped with MC dyes (7). A
mechanism was suggested based on vectorial proton pumping
conducted by light-induced cycle of reversible conformational
transitions (5). Vectorial proton pumping proceeds via confor-
mational transitions in the dye molecule, facilitated by an
acidic proton source. Specifically, the researchers showed
photovoltage generation across membrane-like thin films con-
sisting of oxidized cholesterol and MC in an acidic solution
(7–9).
Different MC dyes are distinguished by their N-alkyl group
substituents. Their chemical structures have a specific symmetry
that causes variations in their binding and crystal structure fol-
lowed by differences in the isomerization temperature, reaction
mode, and the enthalpies involved (10).
In this manuscript, first we reproduced the conventional hex-
adecyl MC photoelectrochemical cell previously reported by
Dutta and Nandy (8) to reiterate the proton pumping capability
of the hexadecyl MC dye. Furthermore, we designed a new pho-
toelectrochemical cell with hexadecyl MC dye embedded in lipid
molecules in which both the current density and the open circuit
voltage improved significantly in comparison to the conventional
hexadecyl MC photoelectrochemical cell. Although there were
isolated reports on the application of MC dyes as a proton pump
membrane to generate photovoltage about two–three decades
ago, to our knowledge, the effort was not pursued further. Our
studies lend further support to the feasibility of using optical and
thermal energy to generate pmf across a macromolecular mem-
brane to design a new high-performance class of MC photoelect-
rochemical cell.
Light induced cis/trans isomerization in the family of merocy-
anine (MC) dyes offers a recyclable proton pumping ability
which can potentially be used in hybrid bio-electronic
devices. In this article, a hexadecyl MC dye is embedded in
lipid molecules to make a macromolecular configuration of a
lipid/hexadecyl MC membrane. Lipid molecules play a criti-
cal role in stabilizing the dye in a membrane structure for
practical use in energy devices. In this study, we first exam-
ined the proton pumping characteristic of the lipid/hexadecyl
MC membrane in a conventional photoelectrochemical cell.
Next, a major modification in the cell was introduced by
eliminating I2/I-electrolyte which resulted in
a two-fold
increase in the open circuit voltage compared with that of
the conventional cell. In addition, the charging time in the
new cell was reduced approximately four orders of magni-
tude. This research demonstrated that the newly designed
lipid- MC cell can act as a promising bioelectronic device
based on the green energy of photoinduced MC dye proton
pumping.
INTRODUCTION
An essential ingredient of biological information processing and
energy transduction is proton motive force (pmf). Several essen-
tial photoinduced biological procedures and dye probed lipid
macromolecules work based on photoisomerization proton pump-
ing and electron transfer mechanisms (1–4). Therefore, creation
of artificial stable systems that allow a light driven trans-mem-
brane proton pump to be interfaced to an electrically active sup-
port is highly desirable.
Photo induced functional incorporation of merocyanine (MC)
dyes embedded in lipid biopolymers promises a novel class of
proton pumps. Such proton pumps open new opportunities in
developing novel bio-inspired devices. Although most dyes are
only sensitive to light, MC dyes belong to the family of both
thermo- and photosensitive molecules. They can cycle between
cis and trans isomeric states via protonation and deprotonation
reactions induced by heat or light (5–7).
MATERIALS AND METHODS
Hexadecyl MC (HMC) dye was synthesized in our laboratory according
to the previously reported method by Minch and Shah (11).
The resulting material was analyzed by X-ray diffraction measurement
(XRD) using Bruker AXS D8 diffractometer. This instrument worked
with voltage and current settings of 40 kV and 40 mA, respectively and
ꢀ
used Cu-Ka radiation (1.5405 A). For qualitative analysis, XRD diagrams
were recorded in the interval 15° ≤ 2h ≤ 55°.
Proton nuclear magnetic resonance (1H NMR) spectroscopy
(600 MHz Bruker) was used to structurally characterize the synthesized
hexadecyl MC dye.
*Corresponding author email: Daryoosh.vashaee@okstate.edu (Daryoosh Vashaee)
© 2013 The American Society of Photobiology
517

518 Lobat Tayebi et al.
To investigate the absorption spectra of hexadecyl MC, the spectro-
photometer Nanodrop 2000 was used. The solvent was acetone and the
concentration of hexadecyl MC in acetone was 10ꢀ5 M.
Cholesterol (95%) was purchased from Alfa Aesar. The oxidized cho-
lesterol was produced by heat and UV oxidation of cholesterol and
recrystallization from n-octane. Pure graphite (99.999%) in appropriate
rod shape was purchased from VWR international to use as electrodes. 1-
palmitoyl-2-oleoyl-sn-glycero-3-phosphocholine (POPC) was purchased
from Avanti Polar Lipid. Thin glass filter (membrane) with 1 lm pores
in average diameter was purchased from VWR international.
toluene, ethanol, methanol, benzyl alcohol, acetonitrile, etc. show
different absorption spectra; and there is always a shift in the
main peaks of MC at 567 nm due to the change in transition
energy and polarity. The main peaks of MC dye in those sol-
vents that keep the polarity of the dye are in a range of 380–
400 nm and 560–620 nm (7,13–17). It was also reported that
hexadecyl MC with acetonitrile as solvent has absorption peaks
in 375 and 580 nm (18).
To investigate the absorption spectra of hexadecyl MC, we
used acetone as the solvent. The concentration of hexadecyl MC
in acetone was 10ꢀ5 M. As Fig. 1C shows, hexadecyl MC in
acetone has two absorption peaks at 394 and 507 nm.
To examine the proton pumping characteristic of hexadecyl
MC dye, two different photoelectrochemical cells were designed.
The first cell was previously introduced by Dutta and Nandy (8).
We made a similar configuration as shown in Fig. 2A. It was
composed of two L-shaped glass tubes connected with standard
joints. A porous glass filter (membrane) with pores of 1 lm
average diameter was mounted in the middle separating the
liquid in the two tubes.
One of the tubes was filled with 0.1 M HCl and the other one
was filled with saturated I2/Iꢀ solution in 0.1 mM concentration.
Also, two graphite electrodes were placed symmetrically one in
each tube. Here, HCl and I2/Iꢀ solution act as proton source and
charge acceptor, respectively. The new configuration of photo-
electrochemical cell is schematically shown in Fig. 2B. As
depicted in this figure, the cell is composed of two graphite elec-
trodes. However, instead of two different electrolytes, both elec-
trodes are immersed in HCl solution, and a glass micro-pored
filter is attached to the cathode.
RESULTS
The 1H NMR data reveal the presence of the hexadecyl MC
product (Fig. 1A). Described by Morley et al. (12), this com-
pound exists as a resonance hybrid with the zwitterionic form
being the predominate structure.
Figure 1B shows the XRD plot of the synthesized HMC dye at
room temperature. All the distinct diffraction peaks at 16.59°,
20.77°, 23° and 29.03° were very prominent and referred to the
crystalline phase of HMC, which is in agreement with the reported
data by Das et al. (9). According to the synthesis procedure, the
cooling process of the final reaction mixture yielded blue-red
crystals which were recrystallized three times from hot water.
Herein, the average crystallite size was determined from the half-
width of diffraction major peaks using the Debye–Scherrer’s
formula (7):
D ¼ kk=b cos h
ð1Þ
where D is the crystallite diameter, k is a constant (shape factor,
ꢀ
about 0.9), k is the X-ray wavelength (1.5405 A as mentioned
before), b is the full width at half maximum (FWHM) of the dif-
fraction line, and h is the diffraction angle. The FWHM was cor-
rected for the instrument broadening and the average crystallite
size was estimated approximately 39.4 nm.
We also examined the absorption spectra of our synthesized
hexadecyl MC. Generally, MC dyes show different absorption
spectra based on their solvents. Patnaik and Sahu (13) reported
that a wide range of solvents such as water, acetone, benzene,
The mixture of hexadecyl MC dye, POPC and oxidized cho-
lesterol (mole ratio ~2:7:13) was prepared and used in both cells.
Hexadecyl MC dye and POPC were dissolved in chloroform,
and cholesterol was dissolved in n-decane. To prepare the mix-
ture, hexadecyl MC and POPC were first mixed in appropriate
molar ratio. Then, the solution was air-dried for 1 h and kept
under vacuum for 3 h to make sure that no chloroform was
trapped in the mixture. The oxidized cholesterol in n-decane was
Figure 1. (A) Structural Characterization of the synthesized hexadecyl MC by 1H NMR (DMSO, 600 MHz): a = 0.81–0.83 (t, 3H), b, c = 1.20–1.24
(m, 26H), d = 1.73–1.75 (m, 2H), e = 4.07–4.08 (t, 2H), k = 6.03 (d, 2H, J = 9 Hz), h = 6.41 (d, 1H, J = 15 Hz), j = 7.25 (br s, 2H), g = 7.43 (s,
2H), i = 7.62 (d, 1H, J = 15 Hz), f = 8.13 (d, 2H, J = 7.2 Hz). (B) XRD diagram of the synthesized hexadecyl MC. The diffraction peaks at 16.59°,
20.77°, 23° and 29.03° are referred to the crystalline phase of hexadecyl MC. The average crystallite size is approximately 39.4 nm. (C) The absorption
spectra of hexadecyl MC in aceton. Two absorption peaks appeared at 394 and 507 nm. They are spectra of the equilibrium isomers of the material in
our experimental condition. All the experiments in panels A, B and C were performed at room temperature.

Photochemistry and Photobiology, 2014, 90 519
Figure 2. Cross-sectional schematic of the cells, (A) the conventional cell (7), and (B) the newly designed MC photoelectrochemical cell.
added to this mixture to reach the desired molar ratio of hexade-
cyl MC dye:POPC:oxidized cholesterol ~2:7:3. For simplicity,
we call this mixture lipid/hexadecyl MC. For complete mixing,
the mixture of lipid/hexadecyl MC was sonicated for ~15–
20 min. The appropriate concentration of the lipid/hexadecyl MC
mixture in n-decane was approximately 3 mM.
In the first cell, the lipid/hexadecyl MC mixture was brushed
on the micropored filter. The filter was mounted between the two
L-shaped tubes to hold a stable lipid/hexadecyl MC membrane
(19). Although the membrane was micro-porous, the continuous
coating of lipid/hexadecyl MC macromolecules successfully pre-
vented mixing of the two solutions of hydrochloride acid and
I2/I-electrolyte.
The main difference between this cell and that of Ref. (8) was
that we embedded the dye and the oxidized cholesterol in the
POPC lipid molecules.
For the second cell, as shown in Fig. 2B, the micro-pored fil-
ter which was attached to the cathode was brushed by the lipid/
hexadecyl MC mixture to form a stable membrane. The open cir-
cuit voltage between the two electrodes of each cell was mea-
sured upon illumination by visible light provided by a 60 W
incandescent light bulb.
The temperature inside the photoelectrochemical cells after
prolonged exposure to visible light was 24°C (equal to the room
temperature).
DISCUSSION
The hexadecyl MC dye can exist in both polar and non-polar
Figure 3. (A) Structure of the synthesized merocyanine dyes. At the
configurations. Only the polar configuration has proton pumping
presence of oxidized cholesterol and lipid molecules more fraction of the
ability. The role of the oxidized cholesterol and the lipid mem-
brane is to increase the concentration of the polar MC to enhance
the proton transfer. Figure 3A shows the polar and non-polar
configurations of hexadecyl MC dye. In the polar form, the rings
of dye are benzenoid but in the non-polar form both rings are
p-quinoidal (20,21). In the environment containing components
of oxidized cholesterol, the N+ terminal is available for binding
because of the electron-donating character of the cholesterol (8).
Hence, most of the dyes are in the polar form.
dyes are in polar form, which enhances the proton pump function of the
membrane. (B) The complete cycle of the proton transfer mechanism in
merocyanine dye: (I) Trans isomer, MTrans, (II) protonated dye molecule
H+MTrans forms, (III) H+MTrans transforms to H+Mcis, (IV) H+Mcis de-
protonated to Mcis and reverts to Mtrans (i.e. I). The procedure occurs
thermally and/or photochemically. This model was first introduced in
Ref. (5).
known for such configurations (5,22). However, in the specific
molecules of our dye, the trans structure cannot be transformed
to the cis one directly by photoelectrochemical process. The
isomerization has to go through the steps shown in Fig. 2b. First
The cis/trans isomerization for the proton pumping action of
the MC dye is suggested as shown in Fig. 2b. MC dye has a stil-
bene-like resonance structure. Cis/trans isomerization is well

520 Lobat Tayebi et al.
200 mV. This observation unambiguously establishes the feasi-
bility for exploiting the concept of pmf generated by the lipid/
MC macromolecules.
CONCLUSION
In this study, a high-performance photoelectrochemical cell was
designed based on the light induced proton pumping characteris-
tic of hexadecyl MC dye which is embedded in lipid molecules.
This newly designed cell differs from the conventional cell by
eliminating the I2/Iꢀ solution as an electrolyte, which decreases
the internal resistance caused by the slow mobility of protons in
I2/Iꢀ electrolyte. Consequently, the current density and open cir-
cuit voltage were significantly improved in the new photoelectro-
chemical cell. These results demonstrate the enhanced energy
harvesting capability of the stable macromolecular membrane of
lipid/hexadecyl MC.
Figure 4. Capacitor charging curves of the conventional and newly
designed MC photoelectrochemical cells.
the trans structure is protonated. As the resonance structure is
stabilized by having a proton at the oxygen end of the MC in
polar configuration, the protonated structure has a more stilbene-
like characteristic (5,6). Then, H+Mcis is obtained by photoelect-
rochemical process on H+Mtrans. H+Mcis is not stable and easily
loses its proton. The cis structure is returned to the trans config-
uration and the loop repeats (5).
Acknowledgements—We thank Prof. Atul N. Parikh and Aref Shahini for
their helpful discussions and insights. This report is supported by the
Oklahoma Center for Advancement of Science and Technology (grant
no. AR131-054 8161) and the AFOSR under grant no. FA9550-10-1-
0010).
This unique feature of MC cis/trans isomerization enables
unidirectional proton transport; hence, the generation of a tappa-
ble pmf. In both cells, the pumping action of the MC dyes trans-
fers H+ ions from one side of the membrane to the other side
which in turn results in voltage generation. The direction of H+
transport in the new cell is not yet clearly understood and
requires detailed study in the future.
We measured the output power to a capacitive load. In the
first cell, an open circuit voltage of about 0.2 V across the mem-
brane was measured repeatedly in separate experiments (Fig. 4),
which is in agreement with the previously reported values (7).
Note that in the previous method the mixture that is brushed
on the micropore did not contain POPC. Due to the amphiphilic
characteristics of POPC lipid bioplymers, POPC self-assembles
as bilayer membrane. Incorporation of MC and oxidized choles-
terol in this membrane makes a significantly more stable struc-
ture than the mixture without POPC.
As discussed earlier, the configuration of the first cell is con-
ventionally used to show the proton pumping capability of the
MC dye. However, this cell has very large internal resistance
likely because of the slow mobility of the protons in I2/Iꢀ elec-
trolyte. Therefore, a new configuration was designed in which
the I2/Iꢀ electrolyte was eliminated. In this new configuration, as
the membrane is directly in contact with the electrode, protons
immediately reach the cathode and the diffusional complications
are circumvented. This results in a dramatic improvement in the
cell open circuit voltage as well as the storage time. For compar-
ison, Fig. 4 depicts the charging curves of a capacitor measured
for the two cells. It can be seen that the charging time in the
new cell is four orders of magnitude reduced from about
104 min in a conventional configuration to 10 min in a new one.
In addition, the open circuit voltage of the new cell is more than
two-fold higher than that obtained using the conventional config-
uration employing I2/Iꢀ solution. The maximum open circuit
voltage for the cell with new configuration is about 580 mV
whereas this value for the conventional configuration is about
REFERENCES
1. Schulten, K. and P. Tavan (1978) Mechanism for light-driven proton
pump of halobacterium-halobium. Nature 272, 85–86.
2. Oesterhe, D. and W. Stoecken (1973) Functions of a new photore-
ceptor membrane. Proc. Natl Acad. Sci. USA 70, 2853–2857.
3. Bhowmik, B. B., C. Senvarma and P. Nandy (1988) Photoinduced
electron-transfer from lipid to dye in a liposome. Phys. Lett. A 130,
55–57.
4. Bhowmik, B. B., R. Dutta and P. Nandy (1985) Photovoltage gener-
ation in dye-probed bilayer lipid-membranes. Indian J. Chem., Sect
A 24, 1046–1047.
5. Abdel-Kader, M. H. and U. Steiner (1983) A molecular reaction
cycle with a solvatochromic merocyanine dye: An experiment in
photochemistry, kinetics, and catalysis. J. Chem. Educ. 60, 160–
162.
6. Steiner, U., M. H. Abdel-Kader, P. Fischer and H. E. A. Kramer
(1978) Photochemical cis/trans isomerization of a stilbazolium beta-
ine. A protolytic/photochemical reaction cycle. J. Am. Chem. Soc.
100, 3190–3197.
7. Basu, R., S. Das and P. Nandy (1993) Photoinduced proton transport
mechanism in merocyanine-dye-probed planar lipid-membranes.
J. Photochem. Photobiol., B 18, 155–159.
8. Datta, R. and P. Nandy (1990) Role of merocyanine dye as a proton
pump in photovoltage generation. Photochem. Photobiol. 52, 907–
909.
9. Das, S., R. Basu, A. Ghose, M. Minch and P. Nandy (1995) Heat-
induced voltage generation in hexadecyl merocyanine dye-probed
planar lipid-membranes. Dyes Pigm. 27, 333–338.
10. Brown, G. H. (ed.) (1971) Photochromism (Techniques of Chemis-
try), Vol. 3. Wiley, New York.
11. Minch, M. J. and S. S. Shah (1979) Spectroscopic studies of hydro-
phobic association-merocyanine dyes in cationic and anionic
micelles. J. Org. Chem. 44, 3252–3255.
12. Morley, J. O., R. M. Morley, R. Docherty and M. H. Charlton
(1997) Fundamental studies on Brooker’s merocyanine. J. Am.
Chem. Soc. 119, 10192–10202.
13. Patnaik, L. and B. Sahu (1994) Solvent effects on the absorption
spectra of merocyanine dyes. J. Solution Chem. 23, 1317–1330.
14. Xiaochuan, L., K. Sung-Hoon and A. S. Young (2009) Optical prop-
erties of donor-p-(acceptor)n merocyanine dyes with dicyanovinylin-
dane as acceptor group and triphenylamine as donor unit. Dyes
Pigm. 82, 293–298.

Photochemistry and Photobiology, 2014, 90 521
15. Svetlichnyi, V. A., A. A. Ishchenko, E. A. Vaitulevich, N. A. Derev-
yanko and A. V. Kulinich (2008) Nonlinear optical characteristics
and lasing ability of merocyanine dyes having different solvatochro-
mic behaviour. Opt. Commun. 281, 6072–6079.
16. Beata, J., K. Janina and P. Jerzy (2007) Dichromophoric hemicya-
nine dyes. Synthesis and spectroscopic investigation. Dyes Pigm. 74,
262–268.
17. Beata, J., K. Janina, P. Marek and P. C. Jerzy (2003) Hemicyanine
dyes: Synthesis, structure and photophysical properties. Dyes Pigm.
58, 47–58.
19. Mountz, J. M. and H. T. Tien (1978) Photoeffects of pigmented
lipid-membranes in a microporous filter. Photochem. Photobiol. 28,
395–400.
20. Brooker, L., A. C. Craig, D.W.S. Heseltine, P.W. Jonkins and L.L.
Lincoln (1965) Color and constitution. XIII. Merocyanines as solvent
property indicators. J. Am. Chem. Sot. 87, 2443–2450.
21. Benson, H. G. and J. N. Murrell (1972) Some studies of benzenoid-
quinonoid resonance. Part 2. The effect of solvent polarity on the
structure and properties of merocyanine dyes. J. Chem. Sot. Faraday
Trans. 68, 137–143.
18. Zimmermann-Dimer, L. M. and V. G. Machado (2009) Chromogenic
anionic chemosensors based on protonated merocyanine solvatochro-
mic dyes: Influence of the medium on the quantitative and naked-
eye selective detection of anionic species. Dyes Pigm. 82, 187–195.
22. Calvin, M. and H. W. Alter (1951) Substituted stilbenes. I. Absorp-
tion Spectra. J. Chem. Phys. 19, 765–768.